The association of the rs1344706 polymorphism of the ZNF804A gene with EEG rhythm synchronization/ desynchronization parameters during the visual perception of semantic and meaningless verbal information was studied in patients with schizophrenia and schizophrenia spectrum disorders (n = 93) and mentally healthy subjects (n = 93). On reading verbal information, regardless of mental status, subjects with the AA genotype showed lower synchronization of the θ rhythm than carriers of the C allele. As compared with carriers of the C allele, healthy carriers of the AA allele showed lower synchronization of the θ rhythm in the posterior cortical areas of the left hemisphere, no difference in synchronization of the γ rhythm, and desynchronization of the μ rhythm on perception of semantic and meaningless verbal information. Patients carrying the AA variant, as compared with carriers of the C variant, showed a lower degree of μ-rhythm desynchronization, which correlated with the severity of speech disorders on the PANSS. The results obtained here indicate that the rs1344706 polymorphism of the ZNF804A gene has a modulating effect on the neurophysiological characteristics of the reading process and contributes to the variability of clinically expressed speech disorders.
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Agosta, S., Magnago, D., Tyler, S., and Grossman, E., “The pivotal role of the right parietal lobe in temporal attention,” J. Cogn. Neurosci., 29, 805–815 (2017).
Alday, P. M. and Kretzschmar, F., “Speed-accuracy tradeoffs in brain and behavior: Testing the independence of P300 and N400 related processes in behavioral responses to sentence categorization,” Front. Hum. Neurosci., 13, 285 (2019).
Anitha, A., Thanseem, I., Nakamura, K., et al., “Zinc finger protein 804A (ZNF804A) and verbal deficits in individuals with autism,” J. Psychiatry Neurosci., 39, No. 5, 294–303 (2014).
Araki, T., Hirata, M., Yanagisawa, T., et al., “Language-related cerebral oscillatory changes are influenced equally by genetic and environmental factors,” NeuroImage, 142, 241–247 (2016).
Bastiaansen, M. and Hagoort, P., “Oscillatory neuronal dynamics during language comprehension,” Progr. Brain Res., 159, 179–196 (2006).
Becker, J., Czamara, D., Hoffmann, P., et al., “Evidence for the involvement of ZNF804A in cognitive processes of relevance to reading and spelling,” Transl. Psychiatry, 2, No. 7, e136 (2012).
Benjamini, Y. and Hochberg, Y., “Controlling the false discovery rate – a practical and powerful approach to multiple testing,” J. R. Stat. Soc. Ser. B., 57, 289–300 (1995).
Brem, S., Bach, S., Kucian, K., et al., “Brain sensitivity to print emerges when children learn letter-speech sound correspondences,” Proc. Natl. Acad. Sci. USA, 107, No. 17, 7939–7944 (2010).
Carreiras, M., Armstrong, B. C., Perea, M., and Frost, R., “The what, when, where, and how of visual word recognition,” Trends Cogn. Sci., 18, No. 2, 90–98 (2014).
Chang, H., **ao, X., and Li, M., “The schizophrenia risk gene ZNF804A: clinical associations, biological mechanisms and neuronal functions,” Mol. Psychiatry, 22, 944–953 (2017).
De Boer, J. N., van Hoogdalem, M., Mandl, R. C. W., et al., “Language in schizophrenia: relation with diagnosis, symptomatology and white matter tracts,” NPJ Schizophr., 6, No. 1, 1–10 (2020).
Dehaene, S. and Cohen, L., “The unique role of the visual word form area in reading,” Trends Cogn. Sci., 15, No. 6, 254–262 (2011).
DeLisi, L. E., “Historical pursuits of the language pathway hypothesis of schizophrenia,” NPJ Schizophr., 7, 53 (2021).
Dias, E. C., Sheridan, H., Martinez, A., et al., “Neurophysiological, oculomotor, and computational modeling of impaired reading ability in schizophrenia,” Schizophr. Bull., 47, No. 1, 97–107 (2021).
Du, J., Palaniyappan, L., Liu, Z., et al., “The genetic determinants of language network dysconnectivity in drug-naive early stage schizophrenia,” NPJ Schizophr., 7, No. 1, 1–10 (2021).
Ford, J., “Schizophrenia: The broken P300 and beyond,” Psychophysiology, 36, No. 6, 667–682 (1999).
Fraga Gonzalez, G., Van der Molen, M. J. W., Žarić, G., et al., “Graph analysis of EEG resting state functional networks in dyslexic readers,” Clin. Neurophysiol., 127, No. 9, 3165–3175 (2016).
Garagnani, M., Lucchese, G., Tomasello, R., et al., “A spiking neurocomputational model of high-frequency oscillatory brain responses to words and pseudowords,” Front. Comput. Neurosci., 10, 145 (2017).
Garakh, Z., Novototsky-Vlasov, V., Larionova, E., and Zaytseva, Y., “Mu rhythm separation from the mix with alpha rhythm: Principal component analyses and factor topography,” J. Neurosci. Meth., 346, 108892 (2020).
Golimbet, V. E., Garakh, Zh. V., Korovaitseva, G. I., et al., “Relationship between neurotrophic brain factor and serotonin transporter genes and parameters of early components of evoked potentials during passive word perception,” Zh. Vyssh. Nerv. Deyat., 66, No. 5, 556–564 (2016).
Golimbet, V., Garakh, Zh., Zaytseva, Y., et al., “The dopamine receptor D2 C957T polymorphism modulates early components of event-related potentials in visual word recognition task,” Neuropsychobiology, 76, 143–150 (2018).
Goto, T., Hirata, M., Umekawa, Y., et al., “Frequency-dependent spatiotemporal distribution of cerebral oscillatory changes during silent reading: a magnetoencephalographic group analysis,” NeuroImage, 54, No. 1, 560–567 (2011).
Hald, L. A., Bastiaansen, M., and Hagoort, P., “EEG theta and gamma responses to semantic violations in online sentence processing,” Brain Lang., 96, No. 1, 90–105 (2006).
Hauk, O. and Pulvermuller, F., “Neurophysiological distinction of action words in the fronto-central cortex,” Hum. Brain Mapp., 21, 191–201 (2004).
Hederih, J., Nuninga, J. O., van Eijk, K., et al., “Genetic underpinnings of schizophrenia-related electroencephalographical intermediate phenotypes: A systematic review and meta-analysis,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 104, 110001 (2021).
Hess, J. L. and Glatt, S. J., “How might ZNF804A variants influence risk for schizophrenia and bipolar disorder? A literature review, synthesis, and bioinformatic analysis,” Am. J. Med. Genet. B, Neuropsychiatr. Genet., 165B, 28–40 (2014).
Huang, Y., Huang, J., Zhou, Q. X., et al., “ZFP804A mutant mice display sex-dependent schizophrenia-like behaviors,” Mol. Psychiatry, 26, No. 6, 1–19 (2020).
Jeon, Y. W. and Polich, J., “Meta-analysis of P300 and schizophrenia: Patients, paradigms, and practical implications,” Psychophysiology, 40, No. 5, 684–701 (2003).
Kay, S. R., Fizbein, A., and Opler, L. A., “The Positive and Negative Symptom Scale (PANSS) for schizophrenia,” Schizophr. Bull., 13, 261–276 (1987).
Larionova, E. V., Garakh, Zh. V., and Zaytseva, Yu. S., “The mu rhythm in modern research: theoretical and methodological aspects,” Zh. Vyssh. Nerv. Deyat., 72, No. 1, 3–27 (2022).
Lewis, A. G., Wang, L., and Bastiaansen, M., “Fast oscillatory dynamics during language comprehension: Unification versus maintenance and prediction?” Brain Lang., 148, 51–63 (2015).
Lezheiko, T. V., Gabaeva, M. V., Kolesina, N. Yu., and Golimbet, V. E., “Studies of the influence of the 3NF804A gene and birth complications on the clinical features of schizophrenia,” Genetika, 55, No. 6, 701–706 (2019).
Lezheiko, T. V., Gabaeva, M. V., Krikova, E. V., and Golimbet, V. E., “The rs1344706 polymorphism of the 3NF804A gene and the clinical heterogeneity of schizophrenia,” Nauchn. Rezult. Biomed. Issled., 6, No. 1, 51–62 (2020).
Linden, D. E., Lancaster, T. M., Wolf, C., et al., “ZNF804A genotype modulates neural activity during working memory for faces,” Neuropsychobiology, 67, No. 2, 84–92 (2013).
Meyer, L., Grigutsch, M., Schmuck, N., et al., “Frontal-posterior theta oscillations reflect memory retrieval during sentence comprehension,” Cortex, 71, 205–218 (2015).
Moreno, I., de Vega, M., and Leon, I., “Understanding action language modulates oscillatory mu and beta rhythms in the same way as observing actions,” Brain Cogn., 82, No. 3, 236–242 (2013).
Murphy, E. and Benitez-Burraco, A., “Language deficits in schizophrenia and autism as related oscillatory connectomopathies: an evolutionary account,” Neurosci. Biobehav. Rev., 83, 742–764 (2017).
Murphy, E. and Benitez-Burraco, A., “Toward the language oscillogenome,” Front. Psychol., 9, 1999 (2018).
Nicodemus, K. K., Elvevag, B., Foltz, P. W., et al., “Category fluency, latent semantic analysis and schizophrenia: a candidate gene approach,” Cortex, 55, 182–191 (2014).
Novototskii-Vlasov, V. Yu., Analysis of Post-Stimulus EEG Changes Not Detected by the Method of Coherent Accumulation: Dissert. for Master’s Degree in Biological Sciences (2000).
O’Donovan, M. C., Craddock, N., Norton, N., et al., “Identification of loci associated with schizophrenia by genome-wide association and follow-up,” Nat. Genet., 40, No. 9, 1053–1055 (2008).
Oliveira, D. S., Saltuklaroglu, T., Thornton, D., et al., “Mu rhythm dynamics suggest automatic activation of motor and premotor brain regions during speech processing,” J. Neurolinguistics, 60, 101006 (2021).
Palaniyappan, L., Du, J., Zhang, J., and Feng, J., “Reply to: ‘Historical pursuits of the language pathway hypothesis of schizophrenia,’” NPJ Schizophrenia, 7, No. 1, 1–3 (2021).
Pfurtscheller, G. and Lopes da Silva, F. H., “Event-related EEG/MEG synchronization and desynchronization: Basic principles,” Clin. Neurophysiol., 110, No. 11, 1842–1857 (1999).
Pinel, P., Lalanne, C., Bourgeron, T., et al., “Genetic and environmental influences on the visual word form and fusiform face areas,” Cereb. Cortex, 25, No. 9, 2478–2493 (2015).
Poeppel, D., Emmorey, K., Hickok, G., and Pylkkanen, L., “Towards a new neurobiology of language,” J. Neurosci., 32, No. 41, 14125–14131 (2012).
Revheim, N., Corcoran, C. M., Dias, E., et al., “Reading deficits in schizophrenia and individuals at high clinical risk: relationship to sensory function, course of illness, and psychosocial outcome,” Am. J. Psychiatry, 171, No. 9, 949–959 (2014).
Rommers, J., Dijkstra, T., and Bastiaansen, M., “Context-dependent semantic processing in the human brain: Evidence from idiom comprehension,” J. Cogn. Neurosci., 25, No. 5, 762–776 (2013).
Saville, C. W., Lancaster, T. M., Davies, T. J., et al., “Elevated P3b latency variability in carriers of ZNF804A risk allele for psychosis,” Neuro-Image, 116, 207–213 (2015).
Smit, D. J., Boersma, M., van Beijsterveldt, C. E., et al., “Endophenotypes in a dynamically connected brain,” Behav. Genet., 40, No. 2, 167–177 (2010).
Strelets, V. B., Garakh, Zh. V., Mar’ina, I. V., et al., “Temporal characteristics of the initial stages of processing verbal information in heath and schizophrenia,” Zh. Vyssh. Nerv. Deyat., 62, No. 2, 165–173 (2012).
Takashima, A., Ohta, K., Matsushima, E., and Toru, M., “The event-related potentials elicit-ed by content and function words during the reading of sentences by patients with schizophrenia,” Psychiatry Clin. Neurosci., 55, No. 6, 611–618 (2001).
Tang, Y., Wang, J., Zhang, T., et al., “P300 as an index of transition to psychosis and of remission: data from a clinical high risk for psychosis study and review of literature,” Schizophr. Res., 226, 74–83 (2020).
Tao, R., Cousijn, H., Jaffe, A. E., et al., “Expression of ZNF804A in human brain and alterations in schizophrenia, bipolar disorder, and major depressive disorder: a novel transcript fetally regulated by the psychosis risk variant rs1344706,” JAMA Psychiatry, 71, No. 10, 1112–1120 (2014).
Uhlhaas, P. J. and Singer, W., “Oscillations and neuronal dynamics in schizophrenia: the search for basic symptoms and translational opportunities,” Biol. Psychiatry, 77, No. 12, 1001–1009 (2015).
Vanova, M., Aldridge-Waddon, L., Jennings, B., et al., “Reading skills deficits in people with mental illness: A systematic review and meta-analysis,” Eur. Psychiatry, 64, No. 1, e19 (2021).
Vukovic, N. and Shtyrov, Y., “Cortical motor systems are involved in second-language comprehension: evidence from rapid mu-rhythm desynchronization,” NeuroImage, 102, 695–703 (2014).
Xu, T., Stephane, M. and Parhi, K. K., “Multidimensional analysis of the abnormal neural oscillations associated with lexical processing in schizophrenia,” Clin. EEG Neurosci., 44, No. 2, 135–143 (2013).
Zhang, Y., Yan, H., Liao, J., et al., “ZNF804A variation may affect hippocampal-prefrontal resting-state functional connectivity in schizophrenic and healthy individuals,” Neurosci. Bull., 34, No. 3, 507–516 (2018).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 73, No. 1, pp. 38–51, January–February, 2023.
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Garakh, Z.V., Golimbet, V.E., Larionova, E.V. et al. Association of the rs1344706 Polymorphism of the ZNF804A Gene with Induced EEG Rhythm Changes during Visual Perception of Verbal Stimuli in Healthy and Schizophrenic Subjects. Neurosci Behav Physi 53, 846–855 (2023). https://doi.org/10.1007/s11055-023-01477-7
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DOI: https://doi.org/10.1007/s11055-023-01477-7